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Dioecy Is Associated with High Genetic Diversity and Adaptation Rates in the Plant Genus Silene Aline Muyle *,1,2 Hele`ne Martin*,3 ,4 Niklaus Zemp,5,6 Maeva Mollion,7 Sophie Gallina,3 Raquel Tavares,1 Alexandre Silva,8 Thomas Bataillon,7 Alex Widmer,5 Sylvain Glemin,9,10 Pascal Touzet*,3 and Gabriel A.B. Marais†,1 1Laboratoire de Biometrie et Biologie Evolutive (UMR 5558), CNRS/Universite Lyon 1, Villeurbanne, France 2Department of Ecology and Evolutionary Biology, UC Irvine, Irvine, CA 3University of Lille, CNRS, UMR 8198—Evo-Eco-Paleo, F-59000 Lille, France 4 Departement de Biologie, Institut de Biologie Integrative et des Syste`mes, Universite Laval, Quebec, QC, Canada Downloaded from https://academic.oup.com/mbe/article/38/3/805/5905496 by Beurlingbiblioteket user on 17 June 2021 5Institute of Integrative Biology, ETH Zurich, Zurich, Switzerland 6Genetic Diversity Centre (GDC), ETH Zurich, Zurich, Switzerland 7Bioinformatics Research Centre, Aarhus University, Aarhus C, Denmark 8Centro de Interpretac¸~ao da Serra da Estrela (CISE), Seia, Portugal 9CNRS, ECOBIO [(Ecosyste`mes, Biodiversite, Evolution)]—UMR 6553, University of Rennes, Rennes, France 10Department of Ecology and Genetics, Evolutionary Biology Center and Science for Life Laboratory, Uppsala University, Uppsala, Sweden †Present address: LEAF- Linking Landscape, Environment, Agriculture and Food, Instituto Superior de Agronomia, Universidade de Lisboa, Portugal All the RNA-seq reads generated for this study can be downloaded from the European Nucleotide Archive accession PRJEB39526. These authors contributed equally as co-first authors to this work. These authors contributed equally as co-senior authors to this work. *Corresponding authors: E-mails: [email protected];[email protected]; [email protected]; gabriel.- [email protected]. Associate editor: Wright Stephen Abstract About 15,000 angiosperm species (6%) have separate sexes, a phenomenon known as dioecy. Why dioecious taxa are so rare is still an open question. Early work reported lower species richness in dioecious compared with nondioecious sister clades, raising the hypothesis that dioecy may be an evolutionary dead-end. This hypothesis has been recently challenged by macroevolutionary analyses that detected no or even positive effect of dioecy on diversification. However, the possible Article genetic consequences of dioecy at the population level, which could drive the long-term fate of dioecious lineages, have not been tested so far. Here, we used a population genomics approach in the Silene genus to look for possible effects of dioecy, especially for potential evidence of evolutionary handicaps of dioecy underlying the dead-end hypothesis. We collected individual-based RNA-seq data from several populations in 13 closely related species with different sexual systems: seven dioecious, three hermaphroditic, and three gynodioecious species. We show that dioecy is associated with increased genetic diversity, as well as higher selection efficacy both against deleterious mutations and for beneficial mutations. The results hold after controlling for phylogenetic inertia, differences in species census population sizes and geographic ranges. We conclude that dioecious Silene species neither show signs of increased mutational load nor genetic evidence for extinction risk. We discuss these observations in the light of the possible demographic differences between dioecious and self-compatible hermaphroditic species and how this could be related to alternatives to the dead-end hypothesis to explain the rarity of dioecy. Key words: sexual systems, selection efficacy, Allee effect, population genetics, RNA-seq, angiosperms. Introduction which individuals carry bisexual flowers. Nonetheless, dioecy can be found in 40% of angiosperm families. The current Out of 261,750 angiosperm species, 15,600 (6%) are di- view is that many independent (871 to 5,000) and mostly oecious (Renner 2014). Dioecy is thus rare compared with the recent transitions occurred from hermaphroditism to dioecy dominant sexual system in angiosperms, hermaphroditism, in ß The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http:// creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact [email protected] Open Access Mol. Biol. Evol. 38(3):805–818 doi:10.1093/molbev/msaa229 Advance Access publication September 14, 2020 805 Muyle et al. doi:10.1093/molbev/msaa229 MBE in angiosperms (Renner 2014). These events probably fol- dioecy was not associated with an increased extinction rate lowed two main evolutionary paths: one through a gynodioe- (Sabath et al. 2016; Duan et al. 2018). Another hypothesis to cious intermediate (with female and hermaphrodite explain the rareness of dioecy in angiosperms posits that re- individuals), called the gynodioecy pathway, and another version from dioecy to other sexual systems is frequent and one through a monoecious intermediate (with a single indi- that dioecy is more evolutionary labile than previously vidual carrying separate female and male flowers) called the thought (Kafer et al. 2017). This hypothesis was supported monoecy or paradioecy pathway (Barrett 2002). In few cases, by a study of 2,145 species from 40 genera in which the dioecy might have evolved through alternative pathways, authors found evidence of frequent reversions from dioecy such as heterostyly (where individuals have different style to other breeding systems (Goldberg et al. 2017). However, and stamen lengths, Barrett 2002). these works relied on macroevolutionary and comparative Species richness was originally found to be lower in dioe- approaches and the population functioning of dioecious ver- Downloaded from https://academic.oup.com/mbe/article/38/3/805/5905496 by Beurlingbiblioteket user on 17 June 2021 cious compared with nondioecious sister clades, suggesting susnondioeciousspecieshasso far been poorly explored. that dioecy might lead to an increased extinction rate in Investigating consequences both at the macroevolutionary angiosperms and defining the evolutionary dead-end hypoth- and population scale have been fruitful in the study of the esis (Heilbuth 2000). Theoretical work has explored this idea evolution of selfing from outcrossing, another frequent breed- and shown that an increased extinction rate could result from ing system transition in angiosperms. Selfing was also pro- two main evolutionary handicaps (reviewed in Muyle and posed to be an evolutionary dead-end, which has been Marais 2016). First, in dioecious species, only females contrib- supported by several macroevolutionary analyses (Goldberg ute to seed production and dispersal, which could result in et al. 2010; de Vos et al. 2014; Zenil-Ferguson et al. 2019). In individuals being less dispersed spatially and competing more parallel, various negative genetic consequences of selfing (i.e., for local resources compared with populations with her- low genetic diversity, accumulation of deleterious mutations) maphrodites (Heilbuth et al. 2001). This should cause dioe- have been reported in several species, even in those of recent cious species to have smaller geographic distributions and origin (see Glemin et al. 2019 for a review). Interestingly, neg- species abundance compared with nondioecious species. ative genetic consequences have been detected despite the Second, in dioecious species with insect pollination, male short-term advantage of selfing provided by reproductive as- intrasexual competition would result in males being more surance, allowing higher colonization potential and larger attractive than females for pollinators, making reproduction species range (Randle et al. 2009; Grossenbacher et al. 2015). and population size sensitive to variation in pollinator density If the seed-dispersal handicap of dioecy operates, it should (Vamosi and Otto 2002). This should lead to fluctuating pop- reduce the ability of dioecious plants to spread and increase ulation sizes in dioecious species and in turn affect levels of local competition, which should lead to smaller geographic genetic diversity. It has been proposed that these handicaps distributions and lower species abundance in dioecious com- could be the reason why dioecy is associated with a specific pared with nondioecious species. These expectations can be suite of traits in angiosperms (fleshy fruits, wind-pollination, tested using estimates of geographic distributions and species inconspicuous flowers, and woody growth) as well as ecolog- abundance in dioecious and nondioecious species. If the pol- ical preferences because dioecious species are preferentially linator handicap of dioecy exists, it should cause fluctuations found in the tropics and on islands (Vamosi et al. 2003). in dioecious population sizes. The effective population size Assuming that pollination mode evolves more slowly than (Ne) is given by the harmonic mean of the varying population dioecy, dioecy could be more frequent among wind- sizes over time (Wright 1938). The harmonic mean tends to pollinated species because wind-pollinated species are not be dominated by the smallest population sizes that the pop- subject to the pollinator handicap. Similarly, assuming fruit ulation goes through.

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